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Knowledge mapping of induced membrane technique: a scientometric study from 2004 to 2023

Journal of Orthopaedic Surgery and Research volume 19, Article number: 600 (2024) Cite this article

Abstract

Background

The induced membrane technique (IMT) is a two-step procedure used for reconstructing segmental bone defects in the limbs. The osteogenic mechanism after bone grafting using IMT remains unclear, and efforts to modify the original techniques are limited to the investigative phase. Therefore, reviewing existing knowledge and identifying hotspots and new trends in IMT is critical.

Methods

We retrieved reviews and articles associated with IMT published between 2004 and 2023 from the Web of Science Core Collection (WoSCC). The keywords included induced membrane technique, guided bone regeneration, bone defect reconstruction, bone graft, stem cells, Masquelet technique, management of bone defects, and scaffold. HistCite, VOSviewer, CiteSpace, and R-bibliometrics were used for scientometric analysis.

Results

A total of 1019 publications from 374 academic journals with 33,995 co-cited references by 2,331 institutions from 65 countries or regions were included. China (n = 235) and the United States (n = 215) were the most productive countries, with Shanghai Jiao Tong University producing the most number of publications (n = 18). Journal Injury [co-citations = 1774; impact factor (IF) 2022 = 2.5] published the most manuscripts, while Masquelet AC and Giannoudis PV published literature with a significant influence on IMT, showing more co-citations (n = 727; n = 355). Two preface hotspots of IMT focused on investigating the microscopic mechanism (such as the membrane supporting graft-to-bone union and the role of inflammatory cells) and developing new techniques to improve IMT (such as bone tissue engineering and new drugs).

Conclusion

This study comprehensively reviewed the literature about IMT published in the last 20 years using qualitative and quantitative methods, providing valuable information for researchers investigating IMT.

Introduction

Large bone defects resulting from diverse etiologies like severe trauma, infection, or the resection of bone tumors often trouble patients due to the uneasy-healing characteristics of body repair mechanisms [1]. However, effectively repairing large bone defects remains a daunting clinical challenge, as the existing techniques have significant limitations. For example, the Ilizarov technique is complex and time-consuming [2, 3]; autologous bone transplantation with a vascular pedicle is limited by donor site morbidity and availability [4], and the Papineau technique carries the risk of infection and nonunion [5].

The induced membrane technique (IMT), also known as Masquelet technique, was first introduced by a French scholar, Masquelet et al., in 1986 and has proven effective in treating large bone defects, including those extending up to 25 cm in length [6, 7]. Since then, this technique has achieved promising results in treating bone defects of diverse origins, including infections, tumors, and congenital diseases [7,8,9]. In trauma, IMT treats large bone defects from severe fractures, where conventional methods fall short. It involves implanting a cement spacer to induce a vascularized membrane which supplies many osteoprogenitor cells and induces the secretion of key growth factors, followed by loading the defect with cancellous autologous bone graft inside the induced membrane to promote bone healing [6, 10]. For tumors, particularly after resection, IMT reconstructs large skeletal defects, supporting bone graft incorporation and revascularization, thus preserving limb function and providing an alternative to endoprosthetic reconstructions [11, 12]. In infections, especially chronic osteomyelitis, IMT manages infected bone defects by initially using an antibiotic-loaded cement spacer to induce the membrane and deliver local antibiotics, followed by bone grafts after infection control [13, 14]. Moreover, extensive research has been conducted using animal models like goats, rabbits, and rats to evaluate the technique’s effectiveness [15, 16]. These studies have provided insights into the histomorphology and cytokine mechanisms involved, laying a solid theoretical foundation for the broader application of Masquelet technique in clinical practice.

Bibliometrics is a discipline that uses mathematics and statistics to quantitatively analyze literature across different science disciplines [17, 18], as well as different data features of journals, authors, institutions, and regions, assessing research profiles and hotspot trends [19, 20]. VOSviewer, CiteSpace, and the Online Analysis Platform of Literature Metrology are important tools for conducting co-occurrence and cluster analyses of literary data [21,22,23]. These tools not only visualize the knowledge structure and application pattern but also map out the research field’s distribution. The visualized network mapping can help researchers identify the knowledge sources, important turning points, research hotspots, and future research trends in this field [24, 25]. Additionally, scientific research can be valued using the authoritative multidisciplinary journal evaluation tool of the Journal Citation Reports (JCR) [26].

Data source and search strategy

Data were obtained from the Web of Science Core Collection using the following search strategy: TS = (masquelet technique) OR TS = (induced membrane) AND TS = (bone defect) AND Language = English. The search was restricted to articles published between January 1, 2004, and June 30, 2023, and SCIE database sources. The paper types included articles or reviews (Fig. 1).

Fig. 1
figure 1

Flow chart of data collection, screening, and analysis

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Statistical analysis

A set of specialized tools was used to analyze and visualize the extensive literature data. HistroCite (version 12.03.07) was used to extract annual production, publishing languages, and article types. Impact factors (IFs) were obtained from JCR. Other information about journals, scholars, countries or regions, frequently cited journals, scholars, citations, and relevant visual relationships were identified using VOSviewer (1.6.16). The data were represented as distinct nodes. The node size corresponds to the frequency of studies or co-occurrences, while the linkages between nodes represent their associations; the stronger the association, the larger the linkage. Based on different scenarios, the following VOSviewer reader settings were used: full counting as the counting technique and specific thresholds (T) for elements like countries/regions, institutions, journals, authors, and references.

Additionally, Scimago Graphics was used to construct a distribution network for relevant publications. Furthermore, CiteSpace (6.1.R2) was used to investigate and visualize trends and notable scientific works in a particular research direction. CiteSpace helps create a co-occurrence graph of keywords, effectively clustering all keywords. Microsoft Office Excel 2021 was used for data management and trend evaluation.

Results

Annual growth trend of publications

A total of 1,019 related studies were identified, with 911 articles and 108 reviews published between 2004 and 2023. All of these studies were published in English to facilitate data analysis. The annual output of relevant studies has increased consistently from 2004 to 2023, with an average of approximately 51 papers per year. The annual output surpassed 80 papers in recent years, with 2004 having the lowest number of publications (n = 11, 1.08%). More than 80 papers have been published annually since 2017 (n = 95, 9.32%), except for 2018 (n = 74, 7.26%), which peaked in 2020 and 2022 (n = 106, 10.40%). We collected only the relevant literature published in the first half of 2023. However, linear fitting models predict that the total number of studies in 2023 will reach approximately 108, making it the year with the highest number of publications since the start of the dataset in 2004.

Countries/Regions

A total of 1019 articles emerged from collaborations among the 65 countries and regions (Table 1). In terms of article production, four of the top ten countries or regions contributed more than 100 articles each: China (n = 235), the United States (n = 215), France (n = 103), and Germany (n = 101). The contribution of the remaining top 10 countries ranged from 44 to 78 articles, with Japan ranking fifth (n = 78), followed by the UK (n = 58), South Korea (n = 50), Italy (n = 49), Switzerland (n = 49), and Brazil (n = 44). In the corresponding network map, China, the United States, France, and Germany had larger node sizes, denoting their higher publication counts. However, the United States garnered the highest number of citations (n = 8545), followed by China (n = 3790), France (n = 3458), and Germany (n = 2890). Intriguingly, the four countries or regions leading in the number of publications also dominate. Significant and beneficial collaborations were observed among different countries and regions (Fig. 2).

Table 1 The top 10 countries, regions, and institutions involved in IMT research
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Fig. 2
figure 2

Network map of countries (A) and regional distribution (B) related to IMT research

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Institutions

The top 10 institutions are located in five countries or regions, with three-fifths of them situated in China. A total of 21 institutions have published at least 10 papers each. Shanghai Jiao Tong University (n = 18) published the most articles, followed by the University of Bern (n = 17) and the Third Military Medical University (n = 15). Other noteworthy contributors included New York University and Sichuan University (n = 14), the University of Sao Paulo (n = 13), Peking University, Soochow University, Stanford University, and the University of Michigan (n = 12). A co-authorship network was constructed using institutions (41/2,331, 1.76%) that had published three or more papers (T = 3) (Fig. 3). This visualization highlights the largest subnetwork within the dataset. The nodes representing Shanghai Jiao Tong University, the University of Bern, and the Third Military Medical University were significantly larger due to their higher publication counts. This network also revealed positive inter-institutional collaborations. For example, the University of Bern had close collaboration with the Nippon Dental University.

Fig. 3
figure 3

The network map of institutions for IMT research (T = 3)

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Authors and co-cited authors

The identified literature was attributed to 5,695 authors, five of whom published at least ten papers each. Giannoudis PV leads with the most publications (n = 18), Xie Z is second on the list with 13 publications (n = 13), followed by four researchers—Fujioka-Kobayashi M, Giannoudis PV, Henrich D, and Obert, l—having the same number of publications (n = 10) in this domain (Table 2). To construct the co-authorship map, we focused on authors (123/1,019, 12.07%) with at least three publications (T = 3). Figure 4A represents the largest subnetwork, where the node of Xie Z was significantly larger due to the higher number of publications. Several authors had close collaborations with each other.

Co-cited authors refer to those who have been cited together in multiple publications [27]. Twelve of the 24,456 co-cited authors had more than 100 co-citations each. The author with the highest number of co-citations was Masquelet, AC (n = 727), followed by Giannoudis, PV (n = 355), and Pelissier, P (n = 331). The co-citation counts of the other nine leading authors ranged from 103 to 134 (Table 2). Authors (86/38,679, 0.22%) with at least 30 co-citations (T = 30) were selected to construct the co-citation map (Fig. 4B). Masquelet, AC, exhibited the largest node size due to the highest number of co-citations. An active co-citation relationship was observed between Masquelet, AC, and Giannoudis, PV.

Table 2 The top 15 authors and co-cited authors of IMT research
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Fig. 4
figure 4

The network map of authors (A, T = 3) and co-cited authors (B, T = 30) related to IMT research

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Journals and co-cited academic journals

About 1,019 papers were published in 374 academic journals, five of which were based in developed countries and had published at least 15 papers each. Orthopaedics & Traumatology-Surgery & Research had the most papers (n = 48), followed by Injury (n = 32), Journal of Orthopaedic Trauma (n = 31), Clinical Oral Implants Research (n = 19), and Journal of Orthopaedic Research (n = 15) (Table 3). A citation network map was constructed using journals (45/1019, 4.41%) that had published ≥ 50 papers (Fig. 5A). This image shows larger nodes for Injury, Orthopaedics & Traumatology—Surgery & Research, and Journal of Orthopaedic Trauma due to their higher publication counts.

Only six of the 4,526 co-cited academic journals, all from the UK or the United States, garnered more than 1,000 co-citations each. Injury had the most co-citations (n = 1,774), followed by biomaterials (n = 1,569), Journal of Periodontology (n = 1,086), Clinical Orthopaedics and Related Research (n = 1,025), and Clinical Oral Implants Research and Journal of Bone and Joint Surgery American Volume (n = 1,024). Biomaterials had the highest IF among the top 15 co-cited journals. The co-citation network was constructed similar to the citation network map, using journals (165/7,645, 2.16%) that had published ≥ 50 papers (Fig. 5B). In this image, injury and biomaterials are distinguished by their larger node sizes, reflecting their high number of co-citations.

Table 3 The top 15 journals and co-cited journals of IMT research
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Fig. 5
figure 5

The network map of academic journals (A, T = 50) and co-cited academic journals (B, T = 50) for IMT research

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Co-cited references

Co-cited references are those that have been cited jointly by other publications [28]. Out of the 1,019 related publications, 33,995 co-cited references were identified. The top 10 co-cited references are listed in Table 4, each of which has been cited a minimum of 60 times, with four having over 200 citations. At the top of the list is a study by Masquelet AC et al., titled “The concept of induced membrane for reconstruction of large bone defects,” published in Orthopedic Clinics of North America [6] with the highest co-citations (2010, n = 215), followed by Pelissier P et al. in the Journal of Orthopaedic Research (2004, n = 209) [12], Karger C et al. in Orthopaedics & Traumatology-Surgery & Research (2012, n = 119) [13], and Giannoudis PV et al. in Injury (2011, n = 107) [10]. The remaining six references had co-citation counts ranging from 61 to 91 (Table 4). A co-citation map was created by selecting references (46/33,995, 0.14%) with at least 30 co-citations (T = 30). The largest node for “Masquelet AC, 2010, Orthop Clin North Am” indicates its active co-cited relationships with Pelissier P, 2004, j orthop res (Fig. 6).

Table 4 The top 10 co-cited references related to IMT research
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Fig. 6
figure 6

Network map of co-cited references for IMT research (T = 30)

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References with citation burstness

Citation burstness refers to references that have garnered significant attention from scholars in a specific field within a certain timeframe [29, 30]. Using CiteSpace with a minimum burstness duration set to three years, 53 references were identified with strong citation burstness. Figure 7 displays the top 20 references exhibiting the highest levels of burstness, with red and blue bars representing frequently and infrequently cited references, respectively; a single bar equals one year. The red bars indicate instances of citation burstness [30, 31]. Notably, 70% (14/20) of these references exhibited citation burstness in 2015. Among the top 20 references, the highest burstness (n = 8.38) was attributed to the paper by Giannoudis PV et al., titled “Restoration of long bone defects treated with the induced membrane technique: protocol and outcomes”, peaking from 2016 to 2020 [32].

The second most co-cited reference was by Masquelet AC et al., titled “Induced Membrane Technique: Pearls and Pitfalls”, with citation burstness from 2019 to 2023 (n = 7.92) [33]. This was followed by another publication by the same authors, “Very Long-Term Results of Post-Traumatic Bone Defect Reconstruction by the Induced Membrane Technique,” published in Orthopaedics & Traumatology: Surgery & Research, with citation burstness from 2020 to 2023 (n = 6.85) [34]. In summary, the citation burstness strength for the top 20 references ranged from 4.53 to 8.38, while the duration ranged from 3 to 7 years.

Fig. 7
figure 7

Top 20 references with the highest citation burstness. The red and blue bars represent references cited frequently and infrequently, respectively

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Keywords

A total of 543 keywords and 33 clusters were obtained by CiteSpace using keywords and cluster analyses. The top 10 keywords, each appearing at least 90 times, were listed in descending order of frequency: induced membrane technique, guided bone regeneration, bone defect reconstruction, bone graft, stem cells, Masquelet technique, management of bone defect, and scaffold. Nine of these keywords appeared in more than 100 publications, while three of them surpassed 200. The most frequent keyword was the induced membrane technique (n = 269), followed by guided bone regeneration (n = 252) and expression (n = 224). The remaining six keywords were published 109–197 times. A relational map was constructed using CiteSpace according to the frequency of keywords (Fig. 8A). The larger nodes represent higher-frequency keywords in related publications, indicating their importance in this research field. For example, bone defect reconstruction, bone grafts, and guided bone regeneration are indispensable procedures in the Masquelet technique.

Based on keyword frequency, all keywords were grouped into 33 clusters. The top 10 high-frequency clusters were chondral defects, nuclear factor kappa B (NF-κB), the Masquelet technique, bone tissue engineering, activation, osteogenic differentiation, soft tissue defects, collagen membranes, dental implants, and the Ilizarov technique. Eight of these clusters had more than 30 publications. Cluster 0, labeled “chondral defects”, has the highest number of publications (n = 44), followed by “NF-κB” (n = 38), “Masquelet technique” (n = 37), and “bone tissue engineering” (n = 35). The remaining four clusters had publication counts ranging from 31 to 33. A cluster map was constructed using the top 10 clusters with the largest number of keywords (Fig. 8B). As the collected publications often contain many keywords with similar or closely related meanings, clustering these keywords with common features can help us understand the main research directions in this field more intuitively.

Fig. 8
figure 8

Keyword co-occurrence (A) and keyword aggregation analysis (B)

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Discussion

Annual growth trend analysis

Over the last two decades, 1458 institutions from 65 countries and territories have published 1,019 papers in 374 peer-reviewed journals, collectively citing 28,301 references in two languages. The data from 2004 to 2022 indicate a projected surge in publications for the year 2023, with an estimated 108 new studies. This increase primarily pertains to research focused on the Masquelet technique and induced membranes for treating bone defects, especially between 2017 and 2023. Before 2017, the field experienced modest growth, with fewer than 50 related publications per year. However, the period from 2017 to 2023 witnessed an exponential surge in the volume of literature. Both 2020 and 2022 had over 100 publications; the 95 papers published in 2017 alone surpassed the combined total from 2004 to 2017, indicating that this discipline has gained significant traction in the scientific community in recent years.

Countries/regions analysis

The leading contributors to this field of research are concentrated in three geographical areas: East Asia, Europe, and North America. Six of the top 10 countries and regions are developed countries from Europe and North America, underscoring their strong scientific research capabilities. However, it is worth mentioning that China, Japan, and South Korea also demonstrated high levels of research output. For example, China has produced a large volume of literature across various domains in recent years. Although the United States (n = 215) had slightly fewer publications than China (n = 235), it garnered more than twice (n = 8545) as many citations as China (n = 3790), demonstrating the robust impact of American research in this area. Furthermore, since only China and Brazil (among the top 10 contributors) are developing countries/regions, there is a need to strengthen research capacities in developing nations. These countries and regions must actively learn from and collaborate with developed nations to advance the field.

Institutional and journal analysis

The United States is home to half of the top 10 most prolific research institutions in this field, with the University of Michigan leading the list. Furthermore, eight of the top 10 most influential institutions are based in the United States, while the remaining two are in Australia and China. The most cited institution is the University of Washington in the United States, reinforcing the dominant position of the United States in this scientific domain. Therefore, scholars must prioritize forming collaborative relationships with these pivotal institutions.

In our analysis of high-impact journals, Injury was found to publish the most relevant literature, focusing on orthopedic trauma—directly related to induced membrane applications in bone defects or bone damage. Similarly, orthopedic trauma is the focus of the second, third, and sixth most productive journals. While Injury has the most co-citations, it is noteworthy that Biomaterials garners a similar number of co-citations and ranks first in impact among the top 15 co-cited journals despite being only one-sixth as productive. The leading journals are based in Europe or the United States, emphasizing the substantial advantage developed countries hold in this field. Furthermore, our findings revealed a higher frequency of co-citations in journals with high-impact factors, indicating that these journals are integral to the field. Therefore, authors need to prioritize these platforms for both citing and submitting their work.

Keywords analysis

Keywords in this field indicate the primary research directions. For instance, Fenelon M demonstrated that the calcium phosphate cement (CPC) scaffold promoted proliferation and osteo-differentiation of human bone marrow mesenchymal stem cells in vitro, and by designing a 3D-printed scaffold, the CPC/BMP2 scaffold induced bone formation and led to satisfactory healing of the femoral defect in vivo [35]. Moreover, Henrich D. compared various characteristics of membranes induced around femur bone defects to those in subcutaneous pockets and the periosteum [36]. They discovered that these membranes differed significantly in structural properties, blood vessel locations, and overall thickness. Their results indicated that replacing PMMA cement with a bone graft earlier in the Masquelet technique could result in better and quicker bone healing.

In our analysis, 33 clusters were classified into three categories. The first describes the Masquelet technique, the second its clinical applications, and the third the underlying mechanisms. A closer look at keyword frequencies revealed that the Masquelet technique for treating bone defects is significantly associated with osteogenic differentiation and angiogenesis. This could be one of the mechanisms through which the Masquelet technique treats bone defects.

Summary of strengths and limitations of included studies

The studies on the Masquelet technique and induced membranes in bone defects have several strengths. These include the innovation of the Masquelet technique, which provides a viable solution for managing challenging bone defects, and the extensive clinical and experimental research validating its effectiveness. The technique has shown promising results in bone regeneration and repair, offering a new avenue for orthopedic surgery.

However, the included studies also have limitations. Many studies are retrospective in nature, which may introduce bias and limit the generalizability of the findings. There is also variability in the methodologies used across studies, such as differences in patient selection, surgical techniques, and outcome measures, which complicates direct comparisons. Additionally, long-term follow-up data are often lacking, making it difficult to assess the sustained efficacy of the technique. Future research should focus on prospective, multicenter studies with standardized protocols to provide more robust evidence.

Limitation

However, this study has several limitations. The primary constraint is the exclusive reliance on data from the WoSCC, which limits the scope of our analysis despite its comprehensiveness and reliability. Secondly, all data were generated via scientometric software rather than through manual meta-analyses or systematic reviews, which may introduce bias. For instance, invited articles and authors serving on editorial boards can influence the perceived impact of certain studies. Another limitation is that we did not consider the level of evidence in our collected publications. It is crucial to consider the level of evidence of the studies themselves, in addition to analyzing the author, journal, journal impact factor, and citation count. Future advancements in machine learning, natural language processing, and information science are expected to address these limitations.

Conclusion

The research on Masquelet technique and induced membranes in bone defects has advanced rapidly, particularly since 2017. Leading countries such as China and the United States have made significant contributions to this field and fostered collaborations. Renowned researchers, including Xie Z and Masquelet AC, have authored numerous articles that have been widely cited.

Based on the analysis of the articles we collected, future research is expected to focus on induced membranes combined with materials, gene expression, cells associated with induced membranes, and the fundamental mechanisms of the Masquelet technique. Specifically, researchers should prioritize high-quality randomized controlled trials (RCTs) to verify the efficacy of new materials and techniques in various clinical settings. Additionally, longitudinal studies are needed to assess the long-term effectiveness of the Masquelet technique and its modifications. Researchers should also consider integrating multi-omics approaches, such as genomics, proteomics, and metabolomics, to elucidate the biological processes underlying induced membrane formation and function.

The scientometric analysis presented in this paper provides a comprehensive review of significant literature in this field from 2004 to 2023. By adopting these recommendations, future research may enhance the refinement and broader application of the Masquelet technique in clinical practice.

Data availability

No datasets were generated or analysed during the current study.

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Author notes

  1. Wei Zhang and Xiaodong Wu authors contributed equally to this work and are considered as co-first authors.

Authors and Affiliations

  1. Department of Orthopedics, Guangdong Second Provincial General Hospital, No.466 Xingang Zhong Road, Guangzhou, China

    Wei Zhang, Xiaodong Wu, Shuanji Ou, Changpeng Xu, Yong Qi & Yang Yang

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  1. Wei Zhang
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Contributions

Y Y and Y Q put forward the concept of this study and designed this research. W Z wrote the main manuscript text. XD W collected data and performed the statistical analysis. SJ O prepared figures. CP X revised the manuscript. All Authors reviewed the results and approved the final version of the Manuscript.

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Zhang, W., Wu, X., Ou, S. et al. Knowledge mapping of induced membrane technique: a scientometric study from 2004 to 2023. J Orthop Surg Res 19, 600 (2024). https://doi.org/10.1186/s13018-024-05093-0

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Keywords

Journal of Orthopaedic Surgery and Research

ISSN: 1749-799X